Effects of the entomopathogenic fungus, Beauveria bassiana, with adipokinetic hormone, on Myzus persicae and Trialeurodes vaporariorum

Year 2023, Volume: 14 Issue: 2, 105 - 120, 15.01.2024

İsmail Karaca Ozlem (kalkar) Güven Umesh Kumar Gautam Tuğçe Özek

https://doi.org/10.31019/tbmd.1314013

Abstract

The aim of this study was to investigate the effects of the co-application of entomopathogenic fungi (EMFs) and adipokinetic hormone (AKH) on the green peach aphid, Myzus persicae, and the greenhouse whitefly, Trialeurodes vaporariorum. Single and combined applications of two Beauveria bassiana isolates with AKH were tested. The green peach aphid was more susceptible to treatments than the greenhouse whitefly. Mortality rates of 58%, 67%, %95, and 95% were observed for the single and combined applications of BMAUM M6-4 and BMAUM LD 2016, respectively, against M. persicae. The application of these fungi singly and in combination with AKH against T. vaporariorum caused mortality rates of 44%, 68% and 45% and78%, respectively. The protein level measured at 595 nm with the standard, Bovine Serum Albumin (BSA), for M. persicae and T. vaporariorum revealed that the highest level of nutrient mobilization was for the BMAUM M6-4+AKH treatment. The level of carbohydrate (glucose) was slightly higher in the AKH treatments when compared to the control group. The lowest glucose level was measured for the entomopathogenic fungi application, and highest level was determined for the isolates combined with AKH. The mechanism of action of AKH applied with B. bassiana isolates is not fully understood. Therefore, more detailed studies are needed in this area to determine the potential of this promising approach for inclusion in IPM programs for the control of these insect pests.

Keywords

Adipokinetic Hormone, Beauveria bassiana, Entomopathogen fungi, Myzus persicae, Trialeurodes vaporariorum

Supporting Institution

The Scientific and Technological Research Council of Turkey (TUBITAK) 1002 and TUBITAK 2216 (U.K.G.). Tuğçe ÖZEK: This Author is a 100/2000 YÖK PhD Scholar.

Project Number

No. 218O240

Thanks

The authors thanks to employees of the Plant Protection Department of Isparta University of Applied Sciences, Turkey for their material and facility support. Special thanks to Dalibor KODRÍK (Biology Centre, CAS, and Faculty of Science, Institute of Entomology, University of South Bohemia, Branišovská, České Budějovice, Czech Republic) providing some materials and insect hormone.

Entomopatojen fungus, Beauveria bassiana’nın Myzus persicae ve Trialeurodes vaporariorum üzerindeki etkisinin adipokinetik hormon ile arttırılması

Abstract

Bu çalışmanın amacı, adipokinetik hormon (AKH) ile birlikte uygulanan entomopatojen fungusların etkilerini araştırmaktır. Adipokinetik hormon ile tek ve kombine uygulanan Beauveria bassiana izolatları yeşil şeftali yaprak biti, Myzus persicae ve sera beyazsineği Trialeurodes vaporariorum üzerinde test edilmiştir. M. persicae’nin T. vaporariorum’a göre uygulamaya daha duyarlı olduğu bulunmuştur. M. persicae üzerinde BMAUM M6-4 ve BMAUM LD 2016'nın tek ve hormon ile birlikte uygulamasında sırasıyla %58, %67, %95 ve %95 ölüm oranı görülmüştür. Aynı şekilde T. vaporariorum’a bu funguların tek ve hormon ile birlikte uygulanması sonucu sırasıyla %44, %68 ve %45, %78 oranında ölüm gözlenmiştir. M. persicae ve T. vaporariorum'da Bovine Serum Albumin (BSA) standardı ile 595 nm'de ölçülen protein seviyesi, BMAUM M6-4+AKH uygulamasında en yüksek besin mobilizasyonunu ortaya çıkarmıştır. Adipokinetik hormon tedavisinde karbonhidrat (glikoz) düzeyinin kontrol grubuna göre biraz arttığı bulunmuştur En düşük glukoz düzeyi entomopatojen fungus uygulamasında ölçülmekle birlikte, en yüksek düzey adipokinetik hormon tedavisi ile birlikte B. bassiana izolatlarında saptanmıştır. Entomopatojen funguslarla uygulanan AKH'nin etki mekanizması tam olarak anlaşılamamıştır. Bu nedenle, böceklere karşı gelecekteki entegre yönetim stratejileri için bu alanda yapılacak daha ayrıntılı çalışmalara ihtiyaç vardır.

Keywords

Adipokinetik hormon, Beauveria bassiana, Entomopatojen fungus, Myzus persicae, Trialeurodes vaporariorum

Project Number

No. 218O240

References

• Abbott W. S., 1925. A method of computing the effectiveness of an insecticide. Journal of Economic Entomology, 18: 265–267. https://doi.org/10.1093/jee/18.2.265a
• Akmal M., S. Freed, M. N. Malik & H. T. Gu, 2013. Efficacy of Beauveria bassiana (Deuteromycotina: Hypomycetes) against different aphid species under laboratory conditions. Pakistan Journal of Zoology, 45(1): 71-78.
• Baydar R., Ö. Güven & I. Karaca, 2016. Occurrence of entomopathogenic fungi in agricultural soils from Isparta province in Turkey and their pathogenicity to Galleria mellonella (L.) (Lepidoptera: Pyralidae) larvae. Egyptian Journal of Biological Pest Control, 26 (2): 323-327.
• Bodláková K., P. Jedlička & D. Kodrík, 2017. Adipokinetic hormones control amylase activity in the cockroach (Periplaneta americana) gut. Insect Science, 24(2):259-269. https://doi.org/10.1111/1744-7917.12314
• EFSA, 2021. European Food Safety Authority, The 2019 European Union report on pesticideresidues in food. EFSA Journal, 19(4), 6491. https://doi.org/10.2903/j.efsa.2021.6491
• Feng G., B. Chen & H. Yin, 2004. Trials of Beauveria bassiana, Paecilomyces fumosoroseus and imidacloprid for management of Trialeurodes vaporariorum (Homoptera: Aleyrodidae) on greenhouse grown lettuce. Biocontrol Science and Technology, 14 (6): 531-544. https://doi.org/10.1080/09583150410001682269
• Gäde G. & G. J. Goldsworthy, 2003. Insect peptide hormones: a selective review of their physiology and potential application for pest control. Pest Management Science, 59: 1063-1075. https://doi.org/10.1002/ps.755
• Gautam U. K., A. Bohatá, H. A. Shaik, R. Zemek & D. Kodrík, 2020a. Adipokinetic hormone promotes infection with entomopathogenic fungus Isaria fumosorosea in the cockroach Periplaneta americana. Comparative Biochemistry and Physiology, 229: 108677. https://doi.org/10.1016/j.cbpc.2019.108677
• Gautam, U. K., D. Hlávková, H. A. Shaik, I. Karaca, G. Karaca, K. Sezen, & D. Kodrík, 2020b. Adipokinetic hormones enhance the efficacy of the entomopathogenic fungus Isaria fumosorosea in model and pest insects. Pathogens, 9(10):801. https://doi.org/10.3390/pathogens9100801
• Goldsworthy G. J., D. Kodrík, R. Comley & M. Lightfoot, 2002. A quantitative study of the adipokinetic hormone of the firebug, Pyrrhocoris apterus. Journal of Insect Physiology, 48: 1103-1108. https://doi.org/10.1016/s0022-1910(02)00203-2
• Goldsworthy G. J., K. Opoku-Ware & L. M. Mullen, 2005. Adipokinetic hormone and the immune responses of locusts to infection. Annals of the New York Academy of Sciences, 1040: 106-113. https://doi.org/10.1196/annals.1327.013
• Hoffmann K. H. & M. W. Lorenz, 1998. Recent advances in hormones in insect pest control. Phytoparasitica, 26: 323-330.
• Ibrahim E., M. Hejníková, H. A. Shaik, D. Doležel & D. Kodrík, 2017. Adipokinetic hormone activities in insect body infected by entomopathogenic nematode. Journal of Insect Physiology, 98: 347-355. https://doi.org/10.1016/j.jinsphys.2017.02.009
• Ibrahim E., P. Dobeš, M. Kunc, P. Hyršl & D. Kodrík, 2018. Adipokinetic hormone and adenosine interfere with nematobacterial infection and locomotion in Drosophila melanogaster. Journal of Insect Physiology, 107: 167-174. https://doi.org/10.1016/j.jinsphys.2018.04.002
• Jandricic S. E., M. Filotas, J. P Sanderson & S. P. Wraight, 2014. Pathogenicity of conidia-based preparations of entomopathogenic fungi against the greenhouse pest aphids Myzus persicae, Aphis gossypii, and Aulacorthum solani (Hemiptera: Aphididae). Journal of Invertebrate Pathology, 118: 34-46. https://doi.org/10.1016/j.jip.2014.02.003
• Javed K., H. Javed, T. Mukhtar & D. Qiu, 2019. Efficacy of Beauveria bassiana and Verticillium lecanii for the management of whitefly and aphid. Journal of Agricultural Science, 56 (3): 669-674. https://doi.org/10.21162/PAKJAS/19.8396
• Jedlička P., V. Steinbauerová, P. Simek & H. Zahradnickova, 2012. Functional characterization of the adipokinetic hormone in the pea aphid, Acyrthosiphon pisum. Comparative Biochemistry and Physiology Part A, 162: 51-58. https://doi.org/10.1016/j.cbpa.2012.02.004
• Kim J., G. Jeong, J. H. Han & S. Lee, 2013. Biological control of aphid using fungal culture and culture filtrates of Beauveria bassiana. Mycobiology, 41(4): 221-224. https://doi.org/10.5941/MYCO.2013.41.4.221
• Kodrík D., A. Bednárová, M. Zemanová & N. Krishnan, 2015. Hormonal regulation of response to oxidative stress in insects-an update. International Journal of Molecular Sciences, 16: 25788-25816. https://doi.org/10.3390/ijms161025788
• Kodrík D., I. Bártu & R. Socha, 2010. Adipokinetic hormone (Pyrap-AKH) enhances the effect of a pyrethroid insecticide against the firebug Pyrrhocoris apterus. Pest Management Science, 66: 425-431. https://doi.org/10.1002/ps.1894
• Kodrík D., K. Vinokurov, A. Tomčala & R. Socha, 2012. The effect of adipokinetic hormone on midgut characteristics in Pyrrhocoris apterus L. (Heteroptera). Journal of Insect Physiology, 58, 194–204. https://doi.org/10.1016/j.jinsphys.2011.11.010
• Kodrík D., N. Krishnan & O. Habuštová, 2007. Is the titer of adipokinetic peptides in Leptinotarsa decemlineata fed on genetically modified potatoes increased by oxidative stress?. Peptides, 28: 974-980. https://doi.org/10.1016/j.peptides.2007.01.017
• Kodrík D., R. Socha & R. Zemek, 2002. Topical application of Pya-AKH stimulates lipid mobilization and locomotion in the flightless bug, Pyrrhocoris apterus (L.) (Heteroptera). Physiological Entomology, 27: 15-20. https://doi.org/10.1046/j.1365-3032.2002.00261.x
• Lacey L.A., R. Frutos, K. H. Kaya & P. Vails, 2001. Insect pathogens as biological control agents: Do they have a future. Biological Control, 21 (3): 230-248, 2001. https://doi.org/10.1006/bcon.2001.0938
• Lee G. & J. H. Park, 2004. Haemolymph sugar homeostasis and starvation-induced hyperactivity affected by genetic manipulations of the adipokinetic hormone encoding gene in Drosophila melanogaster. Genetics, 167: 311-323. https://doi.org/10.1534/genetics.167.1.311
• Lorenz, M. W., 2003. Adipokinetic hormone inhibits the formation of energy stores and egg production in the cricket Gryllus bimaculatus. Comparative Biochemistry and Physiology Part B, 136: 197–206. https://doi.org/10.1016/S1096-4959(03)00227-6
• Mullen L. M. & G. J. Goldsworthy, 2006. Immune responses of locusts to challenge with the pathogenic fungus Metarhizium or high doses of laminarin. Journal of Insect Physiology, 52: 389-398. https://doi.org/10.1016/j.jinsphys.2005.10.008.
• Plavšin I., T. Stašková, M. Šery, V. Smykal, H. K. Hackenberger & D. Kodrík, 2015. Hormonal enhancement of insecticide efficacy in Tribolium castaneum: Oxidative stress and metabolic aspects. Comparative Biochemistry and Physiology Part C, 170: 19-27. https://doi.org/10.1016/j.cbpc.2015.01.005
• Quesada-Moraga E., E. A. A. Maranhao, P. Valverde-Garcia & C. Santiago-Alvarez, 2006. Selection of Beauveria bassiana isolates for control of the whiteflies Bemisia tabaci and Trialeurodes vaporariorum on the basis of their virulence, thermal requirements, and toxicogenic activity. Biological Control, 36: 274-287. https://doi.org/10.1016/j.biocontrol.2005.09.022
• Rayne R. C. & M. O'Shea, 1997. Neuropeptide biosynthesis: Possible molecular targets for the control of insect pests. The ACS Symposium Series, 658: 292-300.
• Roeder T., 1999. Octopamine in invertebrates. Progress in Neurobiology, 59:533-561.
• Scarborough R. M., G.C. Jamieson, S. J. Kalisz Kramer, G. A. McEnroe, C. A. Miller & D. A. Schooled, 1984. Isolation and primary structure of two peptides with cardioacceleratory and hyperglycaemic activity from the corpora cardiaca of Periplaneta americana. Proceedings of the National Academy of Sciences, 81:5575-5579. https://doi.org/10.1073/pnas.81.17.5575
• Shaik H. A., A. Mishra & D. Kodrík, 2017. Beneficial effect of adipokinetic hormone on neuromuscular paralysis in insect body elicited by braconid wasp venom. Comparative Biochemistry and Physiology Part C, 196: 11-18. https://doi.org/10.1016/j.cbpc.2017.02.011
• Stoscheck C.M., 1990. Quantitation of protein. Methods in Enzymology, 182: 50-68.
• Velki M., D. Kodrík, J. Večera, B. K. Hackenberger & R. Soch, 2011. Oxidative stress elicited by insecticides: a role for the adipokinetic hormone. General and Comparative Endocrinology, 172: 77-84. https://doi.org/10.1016/j.ygcen.2010.12.009.
• Zimmermann G., 1986. The ‘Galleria bait method’ for detection of entomopathogenic fungi in soil. Journal of Applied Entomology, 102:213-215.